Abstract : The endocranial course and the branching pattern of the middle meningeal artery(MMA) were studied using 167 sides of dry skulls and 66 sides of dissecting room cadavers. Using Adachi�fs classification of branching types of the MMA, Type-II was found to occur at highest frequency (35.93%) and Type-I,Type-III were of almost equal frequency(31.73%; 32.33%). The stem length of the MMA was found to be in the range of 3-54mms(mean-19.03 �} 11.68 mm). In 64.22% of the cases the frontal ramus was found to be enclosed in a bony canal. The incidence pattern of the branching types was not comparable to any other races except to the Chinese where the Type-II frequency was comparable ours.

Study of the course and relations of the stem and the branches of the MMA established that the vessel follows a variable course, depending on the stem length, angulation of the stem as well as of the anterior ramus and the width of the greater wing of the sphenoid.

Knowledge of the variability of the course and the branching pattern of the MMA is of practical importance to the neuro-surgeon while ligating the vessel in cases of subdural haemorrhage due to head injury.

The middle meningeal artery (MMA) is the largest of the arteries supplying the meninges. After entering the middle cranial fossa, it divides into an anterior (frontal or the bregmatic) and a posterior (parietal or lamboidal) branches. However some authors (Rothman-1937) have observed that there is usually a third branch (the middle or the obeliac branch) arising either from the anterior or the posterior branch. Guiffrida-Ruggeri (1913) has devised a classification of the branching pattern using the origin of the middle branch as the criterion. (simplified by Adachi-1928, adapted from Falk and Nicholls-1992): Type I- the middle branch arises from the frontal ramus ; Type II- the middle branch arises from the parietal ramus ; Type III two middle branches arise from the both frontal and parietal rami. Usually the anterior branch and occasionally the posterior branch of the MMA is found to be enclosed in a bony canal of varying length (Chandler and Derezinski- 1935; Rothman- 1937). The branching pattern of the MMA has been thoroughly investigated in European (Guiffrida - Ruggeri -1913); Japanese (Adachi -1928); Chinese (Toida-1934) and American white and negroes (Chandler and Derezinski-1935; Rothman-1937).

Descriptions of the course and relations of the MMA to the endocranial surface of the bones of the cranial vault available in the text are scanty and haphazard. During the study of the branching pattern of the MMA we found that the course and relations of the artery did not always confirm to a uniform pattern and varied depending upon a number of factors. Hence a detailed study of the relation of MMA to the endocranial surface of the bones of the cranial vault was undertaken to define various patterns of its course. There have been no reports on the course & branching pattern of the MMA in the Indian literature.

Material & Methods :

Material for this study comprised of 79 sagittal halves of the skulls (of which 70 were two halves of the same skull and the other nine were ?six of right and three of left sides), 47 skull bases (the corresponding calvaria were available for only 12 bases) and 34 dissection room cadavers (total no of sides examined 241). Nine sides were not considered since in five sides the origin of the MMA was anomalous and the other four sides were damaged.

Typing the branching pattern : Only 167 sides have been used for this purpose (79 sagittal halves, 22 sides of skull bases with calvaria and 66 sides of the dissection room cadavers). In each case the grooves formed by the MMA on the endocranial surface of the cranial vault was used. A pencil sketch of the pattern of the grooves was prepared on the paper and the diagram was scored according to Adachi�fs (1928) classification.

The length of the stem of the MMA (from point of entry to the point of bifurcation) the length of the bony canal, wherever found, and the site of the origin of the middle ramus were measured with a sliding caliper to the nearest millimeter.

Orbital branches of the frontal ramus, notching of the foramen ovale and groove for the accessory middle meningeal artery (ACMMA) were also looked for.

Relations of the course of MMA and its branches to the endocranial surface of the cranial vault: only 153 sides (76 sagittal halves and 77 sides of the bases of the skull) have been used for the observations of the course of stem and anterior ramus. In each case the observations were made by measuring following parameters using a sliding caliper to the nearest millimeter (a) length of the stem (see above), the proportion of its relation to the i) squamous temporal (SQT) (ii) spheno-squamosal suture (Sph.Sq.suture) (iii) the greater wing of the sphenoid (GWS) (b) length of the frontal ramus from its origin to the lesser wing of the sphenoid and proportion of its relation to i, ii and iii during its course. (c) angle of the stem to a line drawn coronally through the foramen spinosum (d) angle of the anterior ramus to the stem [(c) and (d) meausred by a protractor] (e) maximum width of the GWS.

The course and the relations of the posterior ramus of the MMA were studied in 166 sides (77 sagittal halves and 89 sides of the bases of the skull).

Results :

Frequency of branching types :?Using Adachi�fs (1928) classification it was found that type II occurred at highest frequency (35.93%) - (total 60 nos : 38 right, 22 left sides). Type I and III were found to occur at almost equal frequency (type I?31.74%-total 50 nos?21 right, 32 left sides; type III ? 32.33%-total 54 nos-27 right, 27 left sides). A significant side predominance was seen in the occurrence of type I and II. In 38.15% of the specimens symmetrical branching was noticed and in 61.84% it was asymmetrical. (See Plate-I, Figs.1,2,3).

Origin of the middle branch :?The middle ramus arose from the frontal branch in 31.74%, from the parietal branch in 35.93% and from both the anterior and the posterior branches in 32.33% of the cases. The middle branches given off by the anterior rami was mostly above the lesser wing of the sphenoid except in 20% where it arose from the anterior ramus below this level. The middle branches arising from the posterior ramus were given off at a mean distance of 39mm from the point of bifurcation of the stem. In three instances two middle branches were given off by the posterior ramus.

Bony canals along the branches of the MMA :?In 64.22% of the cases the bony canals were noticed along the course of the anterior ramus (unilateral ? 16.81% i.e., total: 39 sides ? 16 of right and 23 of left sides, bilateral ? 55 instances 23.71%). In 7.33% of the cases a bony canal was found along the posterior ramus. (13 sides unilaterally (5.6%) four of right side nine of left side; bilateral two cases -0.86%). The mean length of bony canals along the anterior ramus was- 11.65�}6.5mm (range -right side ? 3 ? 30mm; left side 2-26mm). There was no significant side difference in the mean length of the bony canals. In almost all the instances the bony canals along the anterior ramus were located above the LWS. In four instances there were two bony canals along the course of anterior ramus.

Orbital branches of the anterior ramus :?In 43 case unilaterally and 35 cases bilaterally (total no. of sides: 113 ? 48.71%) grooves leading to the orbit from the anterior ramus suggestive of the orbital branches were found. In 47 cases these grooves lead to the lateral end of the superior orbital fissure, in 53 cases they lead to a foramen in the lateral wall of the orbit (foramen meningo - orbitale) and in six cases there were two grooves leading to both of the above. Notching and grooves leading from the foramen ovale in the middle cranial fossa were noticed in 31.32% of the cases (52 out of 166 sides of the macerated skulls scored). The grooves either lead to the groove for the stem of the MMA or the foramen rotundum. In 8 instances there was a small foramen lateral to or in the interval between the foramen ovale and the foramen spinosum. These grooves and the foramina are suggestive of course of ACMMA. (See Plate-II, Figs-4,5,6).

Course and relations of the stem and the anterior ramus of the MMA according to the stem length :

I. In five instances MMA bifurcated at the point of entry into the middle cranial fossa itself (3.27%): In two instances among these cases the course of the anterior ramus was related to the GWS up to the level of LWS. In one instance the course was related to the SQT first, then to the GWS. In two other cases the anterior ramus was related first to the sph.-sq. suture then to the GWS.

II. There were 54 instances (35.39%) of the stem measuring 3-10mm (7.31�}2.04mm). The course of stem and the anterior ramus followed four different patterns: a) in four cases (stem length less than 5mm) the stem was related to GWS and gave off anterior ramus at an angle of 20�‹ ? 40�‹ which continued its course on the GWS. (b) in one instance the stem after a short distance on the GWS (6mm) traversed on the squamous temporal (3mm); the anterior ramus coursed on the GWS and squamous temporal in equal proportions. (c) In five instances the stem bent at an angle of 40-60�‹ and coursed on the sph.sq. suture immediately after its entry. In one instance of these the anterior ramus was given off at an angle of 30�‹ which coursed on the GWS following short course on the SQT. In four other cases the

Fig. 1 : Show middle (MID) branch arising from the anterior (ANT) ramus; there is also an additional middle branch (double arrows) arising from the anterior ramus (Type-I).

anterior ramus coursed on the sph.sq. suture and then on the GWS. (d) In a large number of cases (44 cases ? 16 of right and 28 of the left side) the course of the stem was nearly vertical (50?90�‹) being related to the SQT. In one instance the anterior ramus continued on the SQT only up to the LWS, then coursed on the parietal bone. In 32 cases the course of the anterior ramus was related to the SQT and then to the GWS in the proportion of:23.1-78.38% (SQT): 21.6-76.92% (GWS); width of the GWS was in the range of 10-22mm and the angle of the anterior ramus to the stem was 40-60�‹. In eleven other cases the course of the anterior ramus was as follows: Sph.sq. suture ? GWS (43.86:55.78-7 cases); complete course up to LWS on the sph.sq. suture (angle - of the stem ? 80�‹; anterior ramus to the stem 30-40�‹ ? 2 cases); successively SQT ? sph.sq.suture and GWS (2 cases).

III. In 27 instances (17.65%) the stem length was in the range of 11-20 mm (mean -15.5�}2.9mm): (a) In four instances the stem was related to the GWS for 3-5mm followed by SQT. The anterior ramus in these cases coursed on the SQT followed by GWS [45.8%:53.94% proportions] (b) In 20 cases the angle of the stem was 60-110�‹ being entirely related to the SQT. In only one case among these the anterior ramus coursed successively on the SQT and then GWS (in two - 50 : 50, in 17 other cases 10.5 ? 66.66% : 33.3 ? 89.47% proportions). (c) in three cases the stem coursed on the sph.sq. suture in its entire course. The anterior ramus in one of these cases coursed on sph.sq. suture then GWS. In the other two cases the course of the anterior ramus was entirely related to the GWS.

IV. In 39 instances (25.49%) the stem length was 21-30mm (mean-25.69�}2.76mm): (a) in one case the stem was related to GWS just lateral to the foramen spinosum followed by SQT. The anterior ramus in this case coursed successively on SQT, sph.sq. suture and then GWS. (b) In 25 cases the entire course of the stem was related to SQT. In 20 of these cases the anterior ramus partially coursed on SQT and then on GWS (2 cases- equal proportions, in 18 other cases 2-10mm on the SQT and then on the GWS). In 5 other cases where the stem ended close to the sph.sq. suture the entire course of the anterior ramus was related to GWS. (c) In 5 instances the stem coursed on both the SQT and on the GWS (66.66 ? 91.66% (SQT) : 8.33 ? 33.33% (GWS) respectively). The course of the anterior ramus began and continued on the GWS. (d) in three cases the stem after a course of 8-22mm over the SQT continued vertically on the sph.sq. suture till it branched; the anterior ramus continued on GWS. (e) In 3 cases the stem turned horizontally at 110 ? 140�‹ and coursed on the sph.sq. suture till it branched. The anterior ramus continued entirely on GWS. (f) In one case the stem (angle 50�‹) coursed equally on sph.sq. suture and the GWS; the anterior ramus continued on the GWS. (g) In one case the entire course of the stem (angle 20�‹) and the anterior ramus were related to the GWS.

V. In 28 instances (18.3%) the length of the stem was above 30mm (mean-37.18mm�}6.19): (a) In eight instances the stems were nearly vertical (50 ? 90�‹) and coursed entirely on the SQT ; in seven instances of these, anterior ramus coursed on GWS and in one instance where the stem was nearly 50mm it reached the upper part of the SQT and branched, the anterior ramus continued on the parietal with out touching the GWS. (b)In nine instances the stem was related to SQT and GWS in the ratio of 60.0?88.6% : 11.43 ? 40.0% respectively; the anterior ramus continued on the GWS. (c) In two cases the stem coursed on the SQT for 78.90% of its course and rest on the sph.sq. suture ? the anterior ramus continued on the GWS. (d) In three cases the stem coursed successively on SQT, sph.sq. suture and then on the GWS where it branched ? in two of these cases the anterior ramus continued on the GWS and in the other case (stem length 54mm) the anterior ramus continued directly on the parietal. (e) in five instances the stem was related to sph.sq. suture and GWS in 39.5 ? 78.1%: 21.9 - 60.5% proportions. Except in two cases where anerior ramus continued directly on parietal in other two cases the anterior ramus continued on the GWS. (f) In one case the stem coursed on the portion of the GWS just lateral to the foramen spinosum (5mm then on the sph.sq. suture (26mm), followed by GWS (14mm); the course of the anterior ramus continued on the GWS.

Course and relation of the posterior ramus : The course of the posterior ramus was dependent on (a) the length and direction of the stem and level at which the posterior ramus was given off; (b) the bone of the cranial vault (ie., SQT, GWS or the diagonally cut across the SQT and coursed on the parietal (50 instances, mean stem length ? 10.6�}5.2mm). (c) in 5 instances it vertically ascended and took abrupt backward turn and coursed horizontally on the SQT to reach the inner surface of the parietal (mean length-13.08�}11.13mm); (d) where the posterior ramus was given off at a higher level it either followed the curve of the anterior and superior margins of the SQT at varying distances and reached the parietal bone (41 instances, stem length -21.64�}6.7mm) or it coursed horizontally straight across the SQT below its upper edge (13 instances, mean length - 29.9�}7.56mm) (2). In 23 cases the posterior ramus was given off on the GWS and the course was as follows : (a) in 19 cases it coursed on the SQT (mean stem length -28.76�}9.07mm) (b) in four cases where the branching was above the level of upper border of the SQT on the GWS it coursed on the parietal (mean stem length 25.5�}11.15mm).3). In three instances (mean stem length - 35.6�}2.89mm) it was given off on the parietal and it coursed on the upper edge of the SQT to course again on the parietal. 4). In one instance the course was related entirely to the parietal (stem length-54 mms).

Discussion

Frequency of branching types : Table I shows the comparative racial incidence of the branching types of the MMA : type I and II are almost of the same frequency in most of the series and the type III is of least frequency. Type I occurs in highest frequency among Europeans (59.6%) and lowest amongst American whites (37.7%). Type II occurs in least frequency among Chinese (34%) and highest among American whites (60%). Type III is the least frequent of all types (2.8-9%), highest reported so far is of Chinese series (17.7%). In our series type I and III occurred in almost equal frequency, and type II the highest.

Table - I Comparitive racial incidence of the branching types of MMA

Race (Author-Year)

No of Sides examined

Type-I (percentage-nos)

Type-II (percentage-nos)

Type-III (percentage-nos)

European (Guiffrida-Ruggeri 1913)

119

59.6(71)

37.8(45)

2.5(3)

Japanese (Akiba-1925)

219

43.8(96)

53.4(17)

2.8(6)

Japanese (Adachi-1928)

110

51.0(51)

40(40)

9(9)

Total Japanese

319

46.1(147)

49.2(157)

4.7(15)

Chinese (Toida-1934)

192

48.3(112)

34.0(79)

17.7(41)

American (i) white

191

37.7(72)

60.2(115)

2.1(4)

(ii) Negro (Rothman-1937)

212

41.5(88)

55.7(118)

2.8(6)

South Indian (Present series)

167

31.74(53)

35.93(60)

32.33(54)

Sex and side predominance : Studies on American (white & negroes ? Rothman-1937) Japanese (Akiba 1925; Adachi-1928) and Italian (Guiffrida-Ruggeri-1913) series have not demonstrated any sex predominance in the branching types. Type II is the most common in American white & negro series of both sexes and Japanese females. Type I is the most frequent in both sexes of the European series (Italians ? Guiffrida ? Ruggeri-1913) In the male Japanese there is only a slight predominance of type I. We could not study the sex predominance in our series as the skulls used were not of known sex and among the cadavers there were only few female specimens. The results of studies on side predominance in other series shows approximately same incidence of all the three types. Toida 1934 did not compare the side incidence of various types in Chinese series (Rothman ? 1937). We observed in our series type II branching occurring at a higher frequency on the right side, type I on the left side and the type III at an equal frequency on both the sides.

A new description of the variations of the MMA has been attempted by Klisovic, Sikic and Krmpotic-Nemanic (1993). They have identified nine variations of the MMA, the last two of which involve the origin of the MMA from the ophthalmic artery. The other seven are based on the relations of the parietal and petro squamous branches to three osseous ridges (juga cerebralia) produced by superior, inferior temporal and the occipito-temporal sulci;type-I (50%)-the parietal branch runs in the upper field (area between upper and middle ridges); type-II (22%)-the parietal branch is missing and the petro-squamous branch gives the obelic and the lambdoid branches; type-III (7%)-two parietal branches are present one above and the other below the upper ridges; type-IV (6%)-the parietal branches run between the middle and the lower ridges; type-V (5%)- a common parieto-petro squamous branch is present; type-VI (5%)-parietal and petro squamous branches are situated in the upper and inferior fields respectively; type-VII (3%)-the parietal branch is situated along the middle ridge. This method was not attempted in this study because the cerebral ridges were not well marked in our specimens.

Chandler and Derezinski (1935) found two cases out of 1200 examined by them of MMA entering through the foramen ovale. In no other series including ours there were instances of MMA entering through the foramen ovale. Rothman (1937) in his series found that the branching distance (stem length) varied between 1-46mm. In our series the stem length varied between 3-54 mms. Except in four cases where the stem terminated at the level of the LWS in all other cases the stem branched below the LWS. Measurement of the branching distance shows that there is no constant distance at which the stem divides into its terminal branches as described in the text books.

The anterior branch was found to originate from the orbit in five cases (2.07%) in our series. Chandler and Derezinski (1935) have reported a 0.7% incidence in their series. The same authors have also reported nine instances of two anterior branches (0.8%). Three different types of variations in course of anterior ramus above the LWS were observed in the present study ? single vessel (46 cases ? 27.54%); bifurcation into two branches (61 cases-36.53%) multiple branches (60 cases-33.93%). No instances of two anterior branches were found.

The posterior ramus : Kanavel and Davies (1922) found 6 different variations in its course (1) the posterior ramus was given off midway between foramen spinosum and the pterion (4%), (2) in 26% it was given off at the level of the pterion, (3) soon after the stem emerging from the foramen spinosum (8%), (4) two posterior ramii at intervals (8%), (5) simultaneously (5%), (6) no posterior branches (two cases). Chandler and Derezinski (1935) found nine variations: (a) single vessel-89.4%; (b) origin near foramen spinosum - 31.5%; (c) origin near the level of GWS -24.7%; (d) midway between b and c -33%; (e) two posterior branches -8.1%; (f) these arose separately -6.6% or g) simultaneously -1.5% h) trifurcation of the posterior ramus- 0.5%. In the present study there were two posterior rami in 56 cases and no instances of its absence.

Incidence of bony canal : Anterior ramus passing through the bony canal for some part of its course is of importance to the neurosurgeon while turning back a bony flap since artery may be injured during this process. Incidence of bony canal in different series is as follows : American (Chandler and Derezinski ? 1935; bilateral 225 / 542 ? 41.5% ; unilateral 211/542 ? left 108 (51.2%); right 103 (48.8%) length 1 ? 30mm); Japanese- (Akiba ? 1925: unilateral 54%; bilateral 46%; length 1-10mm); Chinese (Toida-1934: 58% total; length 1-41mm); American (Rothman-1937): whites (191 sides) ? unilateral-31%, bilateral-69%; Negroes (212 sides) unilateral-41%; bilateral-59%; length-10mm ave-rage). The presence of canal was more frequent in females than males.

Toida (1934) did not find any canal along the posterior ramus where as Rothmans (1937) found three instances and in the present study it was noticed in 7.33% of the cases. Chandler and Derezinski (1935) found in 14.2% of their series an orbital branch arising from the anterior trunk. We found this branch in 48.71% of our series which was passing into the superior orbital fissure in 47 sides or through the foramen meningo-orbitale in 53 cases. Diamond (1991) in a study of orbital arterial homologies has identified these vessels as sphenoidal artery and the meningo-lacrimal artery respectively.

Text book of surface and radiological anatomy (Hamilton, Simon and Ian Hamilton-1971) mentions that MMA divides at or above the level of zygomatic arch. In the present study it was found that except in four cases where the stem divides at the level of LWS in all other cases the branching was located well below the level of the zygomatic arch. Measurement of the stem length shows that there is no constant distance at which the stem terminates into its branches. This fact is of importance to the neurosurgeon since it is likely to lead to a frustrating situation while ligating the artery if the descriptions given by the textbooks are relied upon.

Our study shows that the stem length and its angulation decides to which bone of the cranial vault and to what proportion - the stem would be related during its course. Irrespective of the length more vertical direction of the stem resulted in its being related to the SQT and more acutely angulated stems especially if they were longer, were related to the GWS or the sph.sq. suture. Width of the GWS also played a part in deciding the relations of the stem and the anterior ramus but it was secondary to the length and angulation of the stem. In cases where the stem was very long (over 35mm) and branched above the level of the LWS the anterior ramus did not touch the GWS at all. In a few cases where the GWS was very narrow (steno-crotaphy) the anterior ramus coursed entirely on the parietal after the SQT. In a few cases where the pterion was of fronto-temporal type (pterion-en-retourne) the anterior ramus coursed on the fronto temporal suture above the GWS.

In injuries of the MMA, one must be aware of the variations of its branches as well as of its anastomoses. Ligature or clipping of the MMA for bleeding after injury will be totally or partially insufficient in many of these cases of variations (Klisovic, Sikic and Krmpotic?Nemanic-1993)

Acknowledgements :

The authors acknowledge the financial grant from the SJMC Research society and the technical assistance by Mr. Jose, Mr. T.S. Satish and Miss Veena Vas.